Journal Home > Volume 15 , Issue 1
Avian Research 2024, 15(1): 100155 https://doi.org/10.1016/j.avrs.2023.100155
Research Article | Open Access | Issue | Published: 28 December 2023

No evidence of predator odor avoidance in a North American bird community

Show Author's Information Austin Dotta,  Batur Yaman,  Alex Van Huynh( )
Department of Biology, DeSales University, 2755 Station Avenue, Center Valley, PA, USA
Keywords:
Foraging, Olfaction, Predation, Odor, Predator-avoidance
Cite this article:
Dotta A, Yaman B, Van Huynh A. No evidence of predator odor avoidance in a North American bird community. Avian Research, 2024, 15(1): 100155. https://doi.org/10.1016/j.avrs.2023.100155
Download citation
EndNote(RIS)
BibTeX

10

Views

0

Downloads

Citations

0

Crossref

0

WoS

0

Scopus

0

CSCD

Abstract Full text About this article

Recent advances in our understanding of avian chemical communication have highlighted the importance of olfaction in many aspects of avian life. Prior studies investigating predator avoidance behaviors in response to predator odor cues have produced mixed results across species and contexts. Here we assess if a community of birds in eastern Pennsylvania displays avoidance behaviors towards predator odor cues in a natural foraging setting. We use clay caterpillars to measure foraging activity by birds in the presence of predator (bobcat) urine, non-predator (rabbit) urine, and water controls in two different environmental contexts (field vs. forest). Although we detected a weak trend for birds to forage less at predator urine-treated sites, we found no significant difference in avian foraging between the site types. We did find that foraging rates between environmental contexts changed significantly over the course of the experiment, with forest sites showing decreasing foraging rates and field sites showing increasing foraging rates. Our results reinforce the published literature that avoidance of predator odors by birds may not be ubiquitous across contexts and species.


menu
Abstract
Full text
Outline
About this article

No evidence of predator odor avoidance in a North American bird community

Show Author's information Austin Dotta, Batur Yaman, Alex Van Huynh( )
Department of Biology, DeSales University, 2755 Station Avenue, Center Valley, PA, USA

Abstract

Recent advances in our understanding of avian chemical communication have highlighted the importance of olfaction in many aspects of avian life. Prior studies investigating predator avoidance behaviors in response to predator odor cues have produced mixed results across species and contexts. Here we assess if a community of birds in eastern Pennsylvania displays avoidance behaviors towards predator odor cues in a natural foraging setting. We use clay caterpillars to measure foraging activity by birds in the presence of predator (bobcat) urine, non-predator (rabbit) urine, and water controls in two different environmental contexts (field vs. forest). Although we detected a weak trend for birds to forage less at predator urine-treated sites, we found no significant difference in avian foraging between the site types. We did find that foraging rates between environmental contexts changed significantly over the course of the experiment, with forest sites showing decreasing foraging rates and field sites showing increasing foraging rates. Our results reinforce the published literature that avoidance of predator odors by birds may not be ubiquitous across contexts and species.

Keywords: Foraging, Olfaction, Predation, Odor, Predator-avoidance

References(70)

Abolaffio, M., Reynolds, A.M., Cecere, J.G., Paiva, V.H., Focardi, S., 2018. Olfactory-cued navigation in shearwaters: linking movement patterns to mechanisms. Sci. Rep. 8, 11590 https://doi.org/10.1038/s41598-018-29919-0.
DOI Google Scholar

Allen, M.L., Wallace, C.F., Wilmers C.C., 2015. Patterns in bobcat (Lynx rufus) scent marking and communication behaviors. J. Ethol. 33, 9-14. https://doi.org/10.1007/s10164-014-0418-0.
DOI Google Scholar

Amo, L., Galván, I., Tomás, G., Sanz, J.J., 2008. Predator odour recognition and avoidance in a songbird. Funct. Ecol. 22, 289-293. https://doi.org/10.1111/j.1365-2435.2007.01361.x.
DOI Google Scholar

Amo, L., Visser, M.E., van Oers, K., 2011. Smelling out predators is innate in birds. Ardea 99, 177-184. https://doi.org/10.5253/078.099.0207.
DOI Google Scholar

Amo, L., Avilés, J.M., Parejo, D., Peña, A., Rodríguez, J., Tomás, G., 2012. Sex recognition by odour and variation in the uropygial gland secretion in starlings. J. Anim. Ecol. 81, 605-613. https://doi.org/10.1111/j.1365-2656.2011.01940.x.
DOI Google Scholar

Amo, L., López-Rull, I., Pagán, I., García, C.M., 2015. Evidence that the house finch (Carpodacus mexicanus) uses scent to avoid omnivore mammals. Rev. Chil. Hist. Nat. 88, 1-7. http://dx.doi.org/https://doi.org/10.1186/S40693-015-0036-4.
DOI Google Scholar

Amo, L., Tomás, G., López-García, A., 2017. Role of chemical and visual cues of mammalian predators in nest defense in birds. Behav. Ecol. Sociobiol. 71, 1-9. https://doi.org/10.1007/s00265-017-2281-9.
DOI Google Scholar

Balthazart, J., Taziaux, M., 2009. The underestimated role of olfaction in avian reproduction? Behav. Brain Res. 200, 248-259. https://doi.org/10.1016/j.bbr.2008.08.036.
DOI Google Scholar

Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models using lme4. J. Stat. Software 67, 1-48. https://doi.org/10.18637/jss.v067.i01.
DOI Google Scholar

Blackwell, B.F., Seamans, T.W., Pfeiffer, M.B., Buckingham, B.N., 2018. European Starling (Sturnus vulgaris) reproduction undeterred by predator scent inside nest boxes. Can. J. Zool. 96, 980-986. https://doi.org/10.1139/cjz-2017-0299.
DOI Google Scholar

Bonadonna, F., Mardon, J., 2010. One house two families: petrel squatters get a sniff of low‐cost breeding opportunities. Ethology 116, 176-182. https://doi.org/10.1111/j.1439-0310.2009.01725.x.
DOI Google Scholar

Bonadonna, F., Sanz-Aguilar, A., 2012. Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition. Anim. Behav. 84, 509-513. https://doi.org/10.1016/j.anbehav.2012.06.014.
DOI Google Scholar

Bowen, W.D., Cowan, I.M., 1980. Scent marking in coyotes. Can. J. Zool. 58, 473-480.
DOI Google Scholar

Caro, S. P., Balthazart, J., Bonadonna, F., 2015. The perfume of reproduction in birds: chemosignaling in avian social life. Horm. Behav. 68, 25-42. https://doi.org/10.1016/j.yhbeh.2014.06.001.
DOI Google Scholar

Caro, S.P., Balthazart, J., 2010. Pheromones in birds: myth or reality? J. Comp. Physiol. A. 196, 751-766. https://doi.org/10.1007/s00359-010-0534-4.
DOI Google Scholar

Caspers, B.A., Hoffman, J.I., Kohlmeier, P., Krüger, O., Krause, E.T., 2013. Olfactory imprinting as a mechanism for nest odour recognition in zebra finches. Anim. Behav. 86, 85-90. https://doi.org/10.1016/j.anbehav.2013.04.015.
DOI Google Scholar

Caspers, B.A., Gagliardo, A., Krause, E.T., 2015. Impact of kin odour on reproduction in zebra finches. Behav. Ecol. Sociobiol. 69, 1827-1833. https://doi.org/10.1007/s00265-015-1995-9.
DOI Google Scholar

Caspers, B.A., Hagelin, J.C., Paul, M., Bock, S., Willeke, S., Krause, E.T., 2017. Zebra Finch chicks recognise parental scent, and retain chemosensory knowledge of their genetic mother, even after egg cross-fostering. Sci. Rep. 7, 1-8. https://doi.org/10.1038/s41598-017-13110-y.
DOI Google Scholar

Coffin, H.R., Watters, J.V., Mateo, J.M., 2011. Odor-based recognition of familiar and related conspecifics: a first test conducted on captive Humboldt penguins (Spheniscus humboldti). PLoS One. 6, e25002. https://doi.org/10.1371/journal.pone.0025002.
DOI Google Scholar

Driver, R.J., Balakrishnan, C.N., 2021. Highly contiguous genomes improve the understanding of avian olfactory receptor repertoires. Integr. Comp. Biol. 61, 1281-1290. https://doi.org/10.1093/icb/icab150.
DOI Google Scholar

Eichholz, M.W., Dassow, J.A., Stafford, J.D., Weatherhead, P.J., 2012. Experimental evidence that nesting ducks use mammalian urine to assess predator abundance. Auk 129, 638-644. https://doi.org/10.1525/auk.2012.12040.
DOI Google Scholar

Ekner, A., Tryjanowski, P., 2008. Do small hole nesting passerines detect cues left by a predator? A test on winter roosting sites. Acta Ornithol. (Wars.) 43, 107-111. https://doi.org/10.3161/000164508X345392.
DOI Google Scholar
Fox, J., Weisberg, S., 2019. An R Companion to Applied Regression, third ed. SAGE, Thousand Oaks, California, USA.

Fracasso, G., Tuliozi, B., Hoi, H., Griggio, M., 2019. Can house sparrows recognize familiar or kin-related individuals by scent? Curr. Zool. 65, 53-59. https://doi.org/10.1093/cz/zoy018.
DOI Google Scholar

Gérard, A., Ganzhorn, J.U., Kull, C.A., Carrière, S.M., 2015. Possible roles of introduced plants for native vertebrate conservation: the case of Madagascar. Restor. Ecol. 23, 768-775. https://doi.org/10.1111/rec.12246.
DOI Google Scholar

Godard, R.D., Bowers, B.B., Morgan Wilson, C., 2007. Eastern bluebirds Sialia sialis do not avoid nest boxes with chemical cues from two common nest predators. J. Avian Biol. 38, 128-131. https://doi.org/10.1111/j.2007.0908-8857.03788.x.
DOI Google Scholar

Golüke, S., Dörrenberg, S., Krause, E.T., Caspers, B.A., 2016. Female zebra finches smell their eggs. PLoS One 11, e0155513. https://doi.org/10.1371/journal.pone.0155513.
DOI Google Scholar

Grieves, L.A., Gilles, M., Cuthill, I.C., Székely, T., MacDougall-Shackleton, E.A., Caspers, B.A., 2022. Olfactory camouflage and communication in birds. Biol. Rev. 97, 1193-1209. https://doi.org/10.1111/brv.12837.
DOI Google Scholar

Griggio, M., Fracasso, G., Mahr, K., Hoi, H., 2016. Olfactory assessment of competitors to the nest site: an experiment on a passerine species. PLoS One 11, e0167905. https://doi.org/10.1371/journal.pone.0167905.
DOI Google Scholar

Gwinner, H., Berger, S., 2008. Starling males select green nest material by olfaction using experience-independent and experience-dependent cues. Anim. Behav. 75, 971-976. https://doi.org/10.1016/j.anbehav.2007.08.008.
DOI Google Scholar

Henry, J.D., 1977. The use of urine marking in the scavenging behavior of the red fox (Vulpes vulpes). Behaviour 61, 82-105.
DOI Google Scholar

Hiltpold, I., Shriver, W.G., 2018. Birds bug on indirect plant defenses to locate insect prey. J. Chem. Ecol. 44, 576-579. https://doi.org/10.1007/s10886-018-0962-0.
DOI Google Scholar

Hutchinson, L.V., Wenze, B.M., 1980. Olfactory guidance in foraging by Procellariiforms. Condor 82, 314-319. https://doi.org/10.2307/1367400.
DOI Google Scholar

Johnson, L.S., Murphy, S.M., Parrish, G.W., 2011. Lack of predator‐odor detection and avoidance by a songbird, the House Wren. J. Field Ornithol. 82, 150-157. https://doi.org/10.1111/j.1557-9263.2011.00317.x.
DOI Google Scholar

Krause, E.T., Krüger, O., Kohlmeier, P., Caspers, B.A., 2012. Olfactory kin recognition in a songbird. Biol. Lett. 8, 327-329. https://doi.org/10.1098/rsbl.2011.1093.
DOI Google Scholar

Krause, E.T., Paul, M., Krüger, O., Caspers, B.A., 2023. Olfactory sex preferences in six Estrildid Finch species. Front. Ecol. Evol. 11, 1000531 https://doi.org/10.3389/fevo.2023.1000531.
DOI Google Scholar

MacDonald, D.W., 1980. Patterns of scent marking with urine and faeces amongst carnivore communities. Symp. Zool. Soc. Lond. 45, 107-139.
DOI Google Scholar

Mahr, K., Nowack, L., Knauer, F., Hoi, H., 2022. Songbirds use scent cues to relocate to feeding sites after displacement: an experiment in great tits (Parus major). Front. Ecol. Evol. 10, 858981 https://doi.org/10.3389/fevo.2022.858981.
DOI Google Scholar

Nguyen, M., McGrath, C., McNamara, C., Van Huynh, A., 2022. Tritrophic interactions with avian predators: the effect of host plant species and herbivore-induced plant volatiles on recruiting avian predators. J. Field Ornithol. https://doi.org/10.1146/annurev-ento-020117-043507.
DOI Google Scholar

Petit, C., Hossaert-McKey, M., Perret, P., Blondel, J., Lambrechts, M.M., 2002. Blue tits use selected plants and olfaction to maintain an aromatic environment for nestlings. Ecol. Lett. 5, 585-589. https://doi.org/10.1046/j.1461-0248.2002.00361.x.
DOI Google Scholar

Pollonara, E., Luschi, P., Guilford, T., Wikelski, M., Bonadonna, F., Gagliardo, A., 2015. Olfaction and topography, but not magnetic cues, control navigation in a pelagic seabird: displacements with shearwaters in the Mediterranean Sea. Sci. Rep. 5, 16486 https://doi.org/10.1038/srep16486.
DOI Google Scholar

Potier, S., Duriez, O., Célérier, A., Liegeois, J.L., Bonadonna, F., 2019. Sight or smell: which senses do scavenging raptors use to find food? Anim. Cognit. 22, 49-59. https://doi.org/10.1007/s10071-018-1220-0.
DOI Google Scholar

Potier, S., 2020. Olfaction in raptors. Zool. J. Linn. Soc. 189, 713-721. https://doi.org/10.1093/zoolinnean/zlz121.
DOI Google Scholar

Roth, T.C., Cox, J., Lima, S., 2008. Can foraging birds assess predation risk by scent? Anim. Behav. 76, 2021-2027. https://doi.org/10.1016/j.anbehav.2008.08.022.
DOI Google Scholar

Rothman, R.J., Mech, L.D., 1979. Scent-marking in lone wolves and newly formed pairs. Anim. Behav. 27, 750-760.
DOI Google Scholar

Rubene, D., Urhan, U., Ninkovic, V., Brodin, A., 2022. Great tits learn odors and colors equally well, and show no predisposition for herbivore-induced plant volatiles. Front. Ecol. Evol. 9, 800057 https://doi.org/10.3389/fevo.2021.800057.
DOI Google Scholar

Saavedra, I., Amo, L., 2018. Insectivorous birds eavesdrop on the pheromones of their prey. PLoS One. 13, e0190415. https://doi.org/10.1371/journal.pone.0190415.
DOI Google Scholar

Shutler, D., 2019. Some important overlooked aspects of odors in avian nesting ecology. J. Avian Biol. 50, e02003 https://doi.org/10.1111/jav.02003.
DOI Google Scholar

Soini, H.A., Schrock, S.E., Bruce, K.E., Wiesler, D., Ketterson, E. D., Novotny, M.V., 2007. Seasonal variation in volatile compound profiles of preen gland secretions of the dark-eyed junco (Junco hyemalis). J. Chem. Ecol. 33, 183-198. https://doi.org/10.1007/s10886-006-9210-0.
DOI Google Scholar

Sonnenberg, B.R., Branch, C.L., Pitera, A.M., Bridge, E., Pravosudov, V.V., 2019. Natural selection and spatial cognition in wild food-caching mountain chickadees. Curr. Biol. 29, 670-676. https://doi.org/10.1016/j.cub.2019.01.006.
DOI Google Scholar

Stanback, M.T., Dove, C.M., Fonda, C., Parkes, P., Ptaschinski, J., 2019. Eastern Bluebirds (Sialia sialis) do not avoid nest cavities containing predator odors. Wilson J. Ornithol. 131, 680-686. https://doi.org/10.1676/18-163.
DOI Google Scholar

Stanback, M.T., Rollfinke, M. F., 2023. Tree Swallows (Tachycineta bicolor) do not avoid nest cavities containing the odors of house mice (Mus musculus). Wilson J. Ornithol. 135, 79-85. https://doi.org/10.1676/22-00045.
DOI Google Scholar

Stanbury, M., Briskie, J., 2015. I smell a rat: can New Zealand birds recognize the odor of an invasive mammalian predator? Curr. Zool. 61, 34-41. https://doi.org/10.1093/czoolo/61.1.34.
DOI Google Scholar

Steiger, S.S., Fidler, A.E., Valcu, M., Kempenaers, B., 2008. Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? Proc. R. Soc. B: Biol. Sci. 275, 2309-2317. https://doi.org/10.1098/rspb.2008.0607.
DOI Google Scholar

Steiger, S.S., Kuryshev, V.Y., Stensmyr, M.C., Kempenaers, B., Mueller, J.C., 2009a. A comparison of reptilian and avian olfactory receptor gene repertoires: species-specific expansion of group γ genes in birds. BMC Genom. 10, 1-10. https://doi.org/10.1186/1471-2164-10-446.
DOI Google Scholar

Steiger, S.S., Fidler, A.E., Kempenaers, B., 2009b. Evidence for increased olfactory receptor gene repertoire size in two nocturnal bird species with well-developed olfactory ability. BMC Evol. Biol. 9, 1-11. https://doi.org/10.1186/1471-2148-9-117.
DOI Google Scholar

Steiger, S.S., Fidler, A.E., Mueller, J.C., Kempenaers, B., 2010. Evidence for adaptive evolution of olfactory receptor genes in 9 bird species. J. Hered. 101, 325-333. https://doi.org/10.1093/jhered/esp105.
DOI Google Scholar

Van Huynh, A., Rice, A.M., 2019. Conspecific olfactory preferences and interspecific divergence in odor cues in a chickadee hybrid zone. Ecol. Evol. 9, 9671-9683. https://doi.org/10.1002/ece3.5497.
DOI Google Scholar

Van Huynh, A., Rice, A.M., 2021. Odor preferences in hybrid chickadees: implications for reproductive isolation and asymmetric introgression. Behav. Ecol. Sociobiol. 75, 1-11. https://doi.org/10.1007/s00265-021-03069-2.
DOI Google Scholar
Van Huynh, A., 2023. No Evidence of Predator Odor Avoidance in a North American Bird Community, Mendeley Data, V1. https://doi.org/10.17632/sfs64vfstp.1.

Whittaker, D.J., Soini, H.A., Atwell, J.W., Hollars, C., Novotny, M.V., Ketterson, E.D., 2010. Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav. Ecol. 21, 608-614. https://doi.org/10.1093/beheco/arq033.
DOI Google Scholar

Whittaker, D.J., Richmond, K.M., Miller, A.K., Kiley, R., Bergeon Burns, C., Atwell, J.W., et al., 2011a. Intraspecific preen oil odor preferences in dark-eyed juncos (Junco hyemalis). Behav. Ecol. 22, 1256-1263. https://doi.org/10.1093/beheco/arr122.
DOI Google Scholar

Whittaker, D.J., Soini, H.A., Gerlach, N.M., Posto, A.L., Novotny, M.V., Ketterson, E.D., 2011b. Role of testosterone in stimulating seasonal changes in a potential avian chemosignal. J. Chem. Ecol. 37, 1349-1357. https://doi.org/10.1007/s10886-011-0050-1.
DOI Google Scholar

Whittaker, D.J., Gerlach, N.M., Soini, H.A., Novotny, M.V., Ketterson, E.D., 2013. Bird odour predicts reproductive success. Anim. Behav. 86, 697-703. https://doi.org/10.1016/j.anbehav.2013.07.025.
DOI Google Scholar

Yang, S.Y., Walther, B.A., Weng, G.J., 2015. Stop and smell the pollen: the role of olfaction and vision of the oriental honey buzzard in identifying food. PLoS One. 10, e0130191. https://doi.org/10.1371/journal.pone.0130191.
DOI Google Scholar

Zannoni, N., Wikelski, M., Gagliardo, A., Raza, A., Kramer, S., Seghetti, C., et al., 2020. Identifying volatile organic compounds used for olfactory navigation by homing pigeons. Sci. Rep. 10, 15879. https://doi.org/10.1038/s41598-020-72525-2.
DOI Google Scholar

Zhang, J.X., Sun, L., Zuo, M.X., 2009. Uropygial gland volatiles may code for olfactory information about sex, individual, and species in Bengalese finches Lonchura striata. Curr. Zool. 55, 357-365. https://doi.org/10.1093/czoolo/55.5.357.
DOI Google Scholar

Zhang, J.X., Wei, W., Zhang, J.H., Yang, W.H., 2010. Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chem. Senses 35, 375-382. https://doi.org/10.1093/chemse/bjq025.
DOI Google Scholar

Zhang, Y.H., Du, Y.F., Zhang, J.X., 2013. Uropygial gland volatiles facilitate species recognition between two sympatric sibling bird species. Behav. Ecol. 24, 1271-1278. https://doi.org/10.1093/beheco/art068.
DOI Google Scholar

Zidar, J., Løvlie, H., 2012. Scent of the enemy: behavioural responses to predator faecal odour in the fowl. Anim. Behav. 84, 547-554. https://doi.org/10.1016/j.anbehav.2012.06.006.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 18 July 2023
Revised: 19 December 2023
Accepted: 20 December 2023
Published: 28 December 2023
Issue date: March 2024

Copyright

© 2023 The Authors.

Acknowledgements

We thank the DeSales University Biology Department and Women for DeSales for supporting this work. We also thank Wendy Maybruck for her logistical support.

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return